Anahid H. Saradjian

Cortical facilitation of proprioceptive inputs related to gravitational balance constraints during step preparation

Several studies have shown that the transmission of afferent inputs from the periphery to the somatosensory cortex is attenuated during the preparation of voluntary movements. In the present study, we tested whether sensory attenuation is also observed during the preparation of a voluntary step. It would appear dysfunctional to suppress somatosensory information, which is considered to be of the utmost importance for gait preparation. In this context, we predict that the somatosensory information is facilitated during gait preparation. To test this prediction, we recorded cortical somatosensory potentials (SEPs) evoked by bilateral lower limb vibration (i.e., proprioceptive inputs) during the preparation phase of a voluntary right-foot stepping movement (i.e., stepping condition). The subjects were also asked to remain still during and after the vibration as a control condition (i.e., static condition). The amplitude and timing of the early arrival of afferent inflow to the somatosensory cortices (i.e., P1-N1) were not significantly different between the static and stepping conditions. However, a large sustained negativity (i.e., late SEP) developed after the P1-N1 component, which was larger when subjects were preparing a step compared with standing. To determine whether this facilitation of proprioceptive inputs was related to gravitational equilibrium constraints, we performed the same experiment in microgravity. In the absence of equilibrium constraints, both the P1-N1 and late SEPs did not significantly differ between the static and stepping conditions. These observations provide neurophysiological evidence that the brain exerts a dynamic control over the transmission of the afferent signal according to their current relevance during movement preparation.

Opposed optimal strategies of weighting somatosensory inputs for planning reaching movements toward visual and proprioceptive targets

Behavioral studies have suggested that the brain uses a visual estimate of the hand to plan reaching movements toward visual targets and somatosensory inputs in the case of somatosensory targets. However, neural correlates for distinct coding of the hand according to the sensory modality of the target have not yet been identified. Here we tested the twofold hypothesis that the somatosensory input from the reaching hand is facilitated and inhibited, respectively, when planning movements toward somatosensory (unseen fingers) or visual targets. The weight of the somatosensory inputs was assessed by measuring the amplitude of the somatosensory evoked potential (SEP) resulting from vibration of the reaching finger during movement planning. The target sensory modality had no significant effect on SEP amplitude. However, Spearmans analyses showed significant correlations between the SEPs and reaching errors. When planning movements toward proprioceptive targets without visual feedback of the reaching hand, participants showing the greater SEPs were those who produced the smaller directional errors. Inversely, participants showing the smaller SEPs when planning movements toward visual targets with visual feedback of the reaching hand were those who produced the smaller directional errors. No significant correlation was found between the SEPs and radial or amplitude errors. Our results indicate that the sensory strategy for planning movements is highly flexible among individuals and also for a given sensory context. Most importantly, they provide neural bases for the suggestion that optimization of movement planning requires the target and the reaching hand to both be represented in the same sensory modality.

Facilitation of cutaneous inputs during the planning phase of gait initiation.

It has been shown that during the planning of a voluntary movement the transmission of cutaneous afferent inputs to the somatosensory cortex is attenuated shortly before the motor output as well as during movement execution. However, it is not known whether the sensory suppression observed during the planning phase (i.e., before any movement execution) is a systemic phenomenon or whether it is dependent on movement context. For example, movements such as step initiation are controlled based on information received from cutaneous receptors in the feet. Because afferent information emerging from these receptors is critical for movement initiation, we hypothesized that suppression of these inputs may not occur during the planning phase prior to gait initiation. To examine this hypothesis we measured the cortical response to somatosensory stimulation during the planning phase of step initiation and during movement execution. Sensitivity to cutaneous stimulation was assessed by measuring the amplitude of the cortical somatosensory-evoked potential (SEP, over the Cz electrode) following electrical stimulations of the plantar sole of one foot. Two stimulations were provided during the planning phase of a step movement and two stimulations during movement execution. It was found that the P50-N80 SEP was facilitated in the early planning phase (-700 ms before motor execution) compared with when participants remained still (control standing task). This mechanism might contribute to an enhanced perception of cutaneous input leading to a more accurate setting of the forces to be exerted onto the ground to shift the bodys weight toward the supporting side prior to foot-off.

Do Gravity-Related Sensory Information Enable the Enhancement of Cortical Proprioceptive Inputs When Planning a Step in Microgravity?

We recently found that the cortical response to proprioceptive stimulation was greater when participants were planning a step than when they stood still, and that this sensory facilitation was suppressed in microgravity. The aim of the present study was to test whether the absence of gravity-related sensory afferents during movement planning in microgravity prevented the proprioceptive cortical processing to be enhanced. We reestablished a reference frame in microgravity by providing and translating a horizontal support on which the participants were standing and verified whether this procedure restored the proprioceptive facilitation. The slight translation of the base of support (lateral direction), which occurred prior to step initiation, stimulated at least cutaneous and vestibular receptors. The sensitivity to proprioceptive stimulation was assessed by measuring the amplitude of the cortical somatosensory-evoked potential (SEP, over the Cz electrode) following the vibration of the leg muscle. The vibration lasted 1 s and the participants were asked to either initiate a step at the vibration offset or to remain still. We found that the early SEP (90–160 ms) was smaller when the platform was translated than when it remained stationary, revealing the existence of an interference phenomenon (i.e., when proprioceptive stimulation is preceded by the stimulation of different sensory modalities evoked by the platform translation). By contrast, the late SEP (550 ms post proprioceptive stimulation onset) was greater when the translation preceded the vibration compared to a condition without pre-stimulation (i.e., no translation). This suggests that restoring a body reference system which is impaired in microgravity allowed a greater proprioceptive cortical processing. Importantly, however, the late SEP was similarly increased when participants either produced a step or remained still. We propose that the absence of step-induced facilitation of proprioceptive cortical processing results from a decreased weight of proprioception in the absence of balance constraints in microgravity.

Independent Early and Late Sensory Processes for Proprioceptive Integration When Planning a Step

Somatosensory inputs to the cortex undergo an early and a later stage of processing which are characterized by an early and a late somatosensory evoked potentials (SEP). The early response is highly representative of the stimulus characteristics whereas the late response reflects a more integrative, task specific, stage of sensory processing. We hypothesized that the later processing stage is independent of the early processing stage. We tested the prediction that a reduction of the first volley of input to the cortex should not prevent the increase of the late SEP. Using the sensory interference phenomenon, we halved the amplitude of the early response to somatosensory input of the ankle joints (evoked by vibration) when participants either planned a step forward or remained still. Despite the initial cortical response to the vibration being massively decreased in both tasks, the late response was still enhanced during step planning. Source localization indicated the posterior parietal cortex (PPC) as the likely origin of the late response modulation. Overall these results support the dissociation between the processes underlying the early and late SEP. The later processing stage could involve both direct and indirect thalamic connections to PPC which bypass the postcentral somatosensory cortex.